colonization and succession in deep-sea ecosystems

TREE vol. 2, no. 12, December 1987

32 Rauser, W.E. and Curvetto, N.R. (19801 Nature 287,563-564 33 Robinson, NJ. and Jackson, P.J. ( 1986) Physiol. Plant. 67,499-506 34 Robinson, NJ. and Thurman, D.A. ( 1986) Proc. R. Sac. London Ser. B 227,493-501 35 lackson, P.I. et al. Proc. Nat1 Acad. Sci. USA (in press 1

Experimenti/ studies reveal generally slow but variable colonization rates in deep-sea soft bottoms. Species successions following biological disturbance appear to be complex and unpredictable, potentially playing a role in structuring these diverse communities. In contrast, physical processes probably play a prominent role in the rapid species turnovers observed at hydrothermal vents. Better information concerning disturbance regimes, recruitment processes and resource utilization is required to elaborate successional mechanisms in both soft-bottom and vent environments.

Fauna1 colonization and succession in deep-sea ecosystems are of interest for reasons both basic and applied. Basic concerns include identification of the processes structuring the speciose soft- bottom communities: are they disturbance mosaics composed of patches in varying stages of succession’r2? The mechanisms controlling the initiation and maintenance of hydrothermal vent populations in their widely dis- persed and unstable habitats3 are also of fundamental interest. In- creasing commercial exploitation of the deep sea is a further reason for studying colonization and succession: how fast will seafloor ecosystems recover following mining of manganese modules4 or of poly- metallic sulfide deposits around hydrothermal vents? Effective en- vironmental management will require knowledge of the rates of these processes.

Despite compelling reasons for studying seafloor colonization and succession, relatively few data are available from deep-sea ecosystems. The remoteness of the deep ocean makes collection of

Craig Smith is at the School of Oceanography WB-IO, University of Washington, Seattle, WA 98195, USA; Robert Hessler is at the Marine Biology Research Division A-002, Scripps Institution of Oceanography, La lolla, CA 92093, USA.

36 Kruckeberg, A.R. ( 1984) California Serpentines: Flora. Vegetation. Geology. Soils and Management Problems, University of California Press 37 Mayr, E. ( 1954) in Evolution as a Process (Huxley, J., Hardy,A.L. and Ford, E.B..eds). pp. 157-180, Allen & Unwin 38 Dover, G. ( 19821 Nature 299, I I l-l I7

Colonization and Succession in Deep-sea Ecosystems

Craig R. Smith and Robert R. Hessler

time-series data particularly chal- lenging, requiring submersibles or sophisticated free-fall equipment. Nevertheless, current research programs are providing insights into the nature of these processes in soft-bottom and hydrothermal vent environments.

Soft-bottom communities Most studies of deep-sea col-

onization have used sediment trays, which are containers of azoic sediment placed on the seafloor. Azoic substrates typically consist of freeze-thawed sediments obtained from the study site5-9 but also include shallow-water and artificial (glass-bead) sediments of varying organic content6r7f9. This in situ placement of defaunated substrates in trays is conceptually simi-

lar to the use of fouling panels to study colonization and succession on hard bottoms.

Sediment-tray results from three widely separated deep-sea locali- ties and a broad range of depths (Table I) yield a number of gener- alities. With occasional exceptions, colonization rates of sediment- dwelling macrofauna (typically polychaetes, crustaceans, and bivalves > 300 km in smallest dimension) are usually low, with even the longest-deployed trays (59 months) having reduced fauna1 abundance. These low rates are surprisingly constant as water depth and substrate type vary (Fig. 1).

Extrapolation of measured colonization rates to background levels of both macrofaunal densities

Table 1. Deep-sea studies of macrofaunal colonization using sediment trays

Depth Tray areaa Deployment times Treatment type Location (ml (cm21 (months) Refs

Northwest 1800 2500 2-26 Azoic indigenous sediment, caged 5,9 Atlantic and uncaged

Glass beads with fish meal, caged

Northwest 3640 2500 2-59 Azoic indigenous sediment, caged 9 Atlantic and uncaged

Glass beads with fish meal, caged and uncaged

Indigenous sediment (untreated)

Northeast 2 160 314 6-l I Azoic indigenous sediment 687 Atlantic Azoic shelf sediment

Northeast 4 I 50 314 6-l I Azoic indigenous sediment 7 Atlantic Glass beads

Glass beads enriched with bacteria, phytoplankton, or corn-meal agar

Eastern I300 2500 5 Azoic indigenous sediment 8 Pacific Azoic indigenous sediment with

ground kelp

aAll trays were IO cm deep.

@ 1987. Elsewer Publfcations iambridqe 0!69-5347,87:$02 00 359


1000

N 800 E

zi a 0-I < 600

Lz 3 Lz5 2 5 400

IY w

z

ii! 200

0 c 0

4944

t A 8

??

8 I I

10 20 MONTHS ON SEAFLOOR

higher rates of colonization, with background levels of abundance, species richness and adult size classes attained within days to weekslOjl I.

The species structure of colonists in deep-sea sediment trays shows less consistency than gross community colonization rates. Trays deployed over the full range of time intervals (2-59 months, Table 2) almost invariably contain significant abundances of species that are rare or absent in background sediments, as well as species that are dominant in the surrounding com- munity5f8.9. Tray respondents that are rare in the background sediment often come from polychaete

To families well known for their oppor- tunism in shallow waterl2, especially if tray sediments are organically enrichedg. However, the identities

Fig. 1. Numerical densities of macrofaunal benthos in colonization trays, initially devoid of macrofauna, de-

of tray colonists at any time or

ployed for varying intervals in the deep sea. Sedi- place are unpredictable, and seem

ments in trays were collected from the study sites, to depend on the patch structure

frozen to kill macrofauna, and replaced on the seafloor of the surrounding community7,9. in trays. Symbols represent the following: closed Thus, while tray experiments indi- triangles, 2160 m in the Northeast Atlantic ‘,? background community densities c. 2800 m-2; open triang-

cate the presence of opportunistic,

les, 4150 m in the Northeast Atlantic7, background or fugitive, species in the deep sea,

densities c. 3600 m-2; closed squares, 1800 m in the they provide little evidence of the Northwest Atlantic5,‘: backeround densities c. 4900 simple successional sequences m-2; open squares, 3b40 m Fn the Northwest Atlanti@, observed in some shallow-water background densities c. 2900 m-% closed circle, 1300 m in the Eastern Pacifica, background densities c. 4 IO0

and terrestrial systems~o,~2,~3

m-2. Modified from Ref. 9. Although sediment-tray experiments indicate slow colonization

and species richness suggest that community recovery within trays may take more than 2-5 years. In addition, macrofaunal populations in trays deployed for months to years are often dominated by juveniles5-9, suggesting that stable age distributions have not been attained2 and that larval recruitment is important in tray colonization. In contrast, sediment trays placed in intertidal and shallow subtidal habitats exhibit much

rates and unpredictable successional patterns, it is difficult to ex- trapolate these results directly to natural community function. By protruding above the seafloor, sediment trays may suffer from a number of artifactsl4; it has thus proven desirable to develop experimental systems that may more closely approximate natural disturbances within the deep-sea floor.

As an initial alternative to sediment trays, parcels of wood, dead

Table 2. Experimental systems that have been used to study colonization and succession in deep-sea so&bottom benthos

Sediment trays” Implanted food fall+ Manipulated biogenic mounds

Tractability Artifacts Natura: analogs Generality

High Moderate High Many? Few Few? Unclear Rare Common Unclear Moderate Broad?

Wsed in Refs 5-9. Wsed in Refs 9, 14-18. <Used in Ref. 21.

fish or macroalgae were placed on the sediment to elicit community disequilibrium (Table 2). The wood parcels yielded surprising results: at a variety of locations, wood- boring bivalves (subfamily Xylo- phagainae) riddled panels in 4-15 months’5,16. These rapidly maturing bivalves are usually absent from seafloor sediment@, and exploit the ephemeral wood habitat in the mode of truly opportunistic species15. By converting wood to more labile organic material, wood borers also cause enrichment of the local sediment community; en- hanced species include opportunists, such as capitellid polychaetes, which also respond to sediment trays9e’6.

Parcels of macroalgae on the deep-sea floor seem to elicit a more varied response than do wood panels. Concentrations of Sargassum in the Northwest Atlan- tic attracted high densities of apparently opportunistic PolY- chaetes, including several of the species that respond to both wood and sediment traysg. Presumably, the decomposing Sargassum caused organic enrichment of near- by sediments. In contrast, kelp ( Macrocystis pyrifera ) parcels placed at 1300 m in the Eastern Pacific were consumed so rapidly by megafaunal ‘herbivores’ that the sediment community evinced only minor alterations after 3-6 weeks (C.R. Smith, PhD dissertation, Uni- versity of California, San Diego, 1983).

Wood and macroalgal experiments allow assessment of the response of deep-sea fauna to sediment enrichment; the empiace- ment of fish carcasses illustrates the alternative consequences of mechanical disturbance. Bait falls in the deep sea attract large aggregations of voracious scaven- gers, which rapidly consume the carrion before much sediment enrichment occurs17. The predom- inant disturbance effect of carcass falls thus appears to be mechanical disruption of the sediment-water interface, leading to reductions in fauna1 abundance and species richness within a meter of treatments9~i7~‘8.

In at least some deep-sea communities, response to such small- scale physical disturbance can be

360


rapid; at 1300 m in the Eastern Pacific, two dominant polychaete species and a normally rare cuma- cean colonized fish-fall sites within 3-6 weeksl8. Most of this colonization resulted from benthic dispersal (i.e. movement on or in the sediment by post-larval stages) and the intensity of immigration was spatially variable. In contrast, a fish-fall experiment at 3600 m in the Northwest Atlantic yielded greatly reduced macrofaunal abundances near the treatment even after one year, implying a community recovery time at this site consistent with the low rates observed in sediment trays9.

Food-fall experiments certainly mimic natural events, but it is unclear how far their results can be generalized to surrounding communities. Falls of wood, macroalgae and large carcasses appear to be spatially rare9f15f17 and all may cause organic enrichment that is unlikely to occur with other types of perturbation. Clearly, either disturbance of infauna is not common in the deep sea, or there are other more common disturbance agents. Direct study of the most frequent disturbances and their community consequences would be useful in determining whether natural perturbations play a role in structuring deep-sea assemblages.

One potentially common source of disturbance in the deep sea is large sediment mounds (5-15 cm tall, 20-100 cm diameter; Fig. 2) formed from the fecal material of megafaunal deposit feeders, such as the holothuroids or echiuran worms that occur in virtually all deep-sea habitats6,t9-2 I. Experi- ments with echiuran mounds in the Eastern Pacific at 1240 m indicate that fecal deposition on these structures can be very rapid, attain- ing rates of 1-2 cm per month*‘; such rapid deposition leads to significant burial disturbance of intertidal benthos**f*‘, and fauna from low-energy deep-sea environments seem likely to be at least as sensitive4. Fauna1 assemblages on these mounds do in fact show evidence of disturbance; total macro- fauna1 abundance is reduced, while apparently opportunistic capitellid and paraonid polychaetes show population enhancement IC.R. Smith, unpublishedl.

Fig. 2. Typical view of the soft-bottom seafloor at 1240 m in the Eastern Pacific. Visible are a large sediment mound (about I5 x 40 cm), several small mounds and pits, and brittle stars in normal postures. The muddy twig-like structures discernible in several areas are the tubes of polychaete worms and the tests of giant protozoans (Foraminifera). The mounds are composed of fecal pellets from echurian worms and are sites of rapid sediment deposition and in- fauna1 disturbance.

The ease with which mounds can be manipulated should facilitate the documentation of colonization dynamics in these structures. Initial experiments with artificial mounds suggest that community response to sediment burial can be relatively rapid; large mounds ( IO x 40 cm) initially devoid of macrofauna reach >50% of background levels of abundance and species richness within 50 days21 (Fig. 3).

In summary, a variety of experimental approaches have yielded some general insights into soft- bottom colonization in the deep sea:

(a) Opportunistic, or fugitive, species do occur in the deep sea and show taxonomic affinities to shallow-water opportunists. Some can respond rapidly (time scale of weeks to months) to disequilibrium conditions, especially organic enrichment.

(bj The species structure of succession is variable, both within and across habitats. Within-site variabil- ity probably results from the predominance of inefficient (e.g. benthicl dispersal modes*4 com- bined with meter-scale community patchiness.

(cl Even during the earliest stages of succession, opportunistic species are likely to coexist with more equilibrium-type (i.e. background 1 species. We may speculate that this coexistence occurs because disturbance intensities are relatively low and chemical gradi- ents are weak in most deep-sea systems, allowing conditions in

newly disturbed patches to fall within the tolerance range of both opportunistic and equilibrium species.

(d) Finally, while certain experiments elicit a rapid response from many species, most approaches suggest that complete recovery from intense disturbance may take months to years. This conclusion is derived from studies of small (deci- meter-scale) disturbances; large, intense perturbations resulting from nodule mining, turbidity currents, and perhaps benthic storms25, may require significantly longer recovery times.

These generalizations allow us to make some predictions concerning the processes structuring soft-

20 I .

Artificial mounds

(after 50 days)

Background

community site!

Colonization tray

latter 140 days)

Fig. 3. Mean 12~~1 abundance (al and species richness Ibl of macrofauna from replicate 100 cm2 core samples (n = number of samples) collected from two artificial mounds (left), five locations in the background community 370 cm from the nearest mound (middle), and a colonization tray of pre-frozen sediment placed on the seafloor for 140 days lright18. Artificial mounds were IO cm high, 45 cm in diameter. and composed of subsurface sediments, initially devoid of macrofauna, obtained from the study site ( I240 m in the Eastern PacificI”. Sampling occurred 50 days after mound emplacement. The rapid macrofaunal response to artificial mounds may result either from upward burrowing 1i.e. resistance to burial) or from colonization by the surrounding sediment fauna. Both of these response modes may be physically restricted by the structure of the colonization tray. With permission from Nature.

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Fig. 4. Hydrothermal vent fauna at 2500 m depth in ‘Rose Garden’ on the Galapagos spreading center, 200 nautical miles east of the Galapagos Islands. The large thicket (background) and clumps of organisms are composed of vestimentiferan worms (Riftia) and mussels (Bathymodiolus) clustered at larger vents. Smaller vent fissures are clogged with mussels, which are replaced by white clams (Calyptogena) as fissures, and presumably vent flows, dwindle (foreground). Crabs fBythograea and Munidopsis) are also visible. The high standing crop is partial testimony to the productivity of vent systems.

bottom assemblages in the deep sea. Given apparent long recovery times, we suspect that disturbance (e.g. from mound building, pit dig- ging, sedimentation events, etc.) are frequent enough to yield systems composed predominantly of patches in varying stages of recovery9,r8. The attraction of a broad array of species, including community dominants, to disturbance sites indicates that background species structure does not preclude a disturbance-mosaic model. The levels of patchiness observed in many deep benthic assemblages are also consistent with disturbance mosaics, especially if disturbances are low in intensity and small in scale9,r8. The available evidence thus suggests that disequilibrium processes, such as disturbance and succession, could well play a role in maintaining the characteristic structure, including high species diversity, of deep-sea assemblages.

Hydrothermal vent communities In contrast to soft bottoms, the

hydrothermal vents occurring atop ocean ridges in the Eastern Pacific are dominated by physical processes. Individual vent fields persist for only a matter of decades; as vents die, new ones appear else- where along the spreading center. The nature and pattern of venting

362

water are likely to change during the brief existence of the vent field*6. Both flow rate and chemistry may be altered by a variety of subterranean processes.

Most of the vent species are en- demic to the vent environment3J7. (We limit this discussion to megafauna because the rest of the fauna is so poorly known.) Because most species are sessile as adults, planktonic dispersal of larvae must be essential for colonization2&30. While planktonic dispersal certainly entails considerable larval mor- tality, particularly through inability to locate vents, the rich productivity permits high fecundity.

Knowledge of colonization events and community changes is sparse because the study of vent systems began very recently and because returns to specific sites are rare. Information comes as much from analysis of spatial differences in community composition as from true time series. Because accom- panying physical parameters were not usually measured, causal rela- tionships are largely inferred.

Some differences in community structure around vents appear closely related to the variations in vent-fluid flux. For example, the abundance and growth form of the giant vestimentiferan worm Riftia, relative to the bivalves Calyp- togena and Bathymodiolus, sug-

gests that Riftia requires a stronger flow of vent water to flourish (Fig. 413’. Where flow rate is high, the vestimentiferan can grow erect, holding its crown above any associ- ated bivalves. If flow is weak, the delicate crown must be held close to the vent opening. Here it may be damaged by the bivalves, allowing them eventually to dominate the limited vent space. Other observa- tions show that under conditions that will no longer support Calyp- togena, Bathymodiolus persists, probably because it is a suspension feeder as well as a host to chemoautotrophic bacteria3r.

A return to the vent field called Rose Garden after six years pro- vided an unusual opportunity to study directly the dramatic successional changes at vents (R.R. Hess- ler, unpublished). Riftia had initially dominated the field (Fig. 4); six years later it was limited to a few clusters and isolated individuals. The populations of suspension feeders (anemones, serpulids, a siphonophore and an enteropneust) surrounding the vent open- ings had also diminished; the siphonophore and enteropneust were virtually absent. In contrast, populations of both Calyptogena and Bathymodiolus had increased markedly, as had an unidentified whelk and the crab Munidopsis.

The decreased abundance of suspension feeders, as well as Rif- tia, at Rose Garden is consistent with the hypothesis of reduced flow: the flux of suspended organic particles would decline, as would the flux of sulfide. Unfortunately, flux was not measured during either visit. it has also been suggested that Bathymodiofus is so effective in sulfide uptake that insufficient quantities reach the Riftia above them32. If these mussels are equally efficient at particle filtration, a simi- lar mechanism could explain the decline of suspension feeders. For species whose populations increased, possible causes include increased nutritive resources, suc- cessful competition for space, and a continuing, slow influx of propa- gules.

In summary, factors affecting planktonic dispersal will be important in the colonization of vents. For settled individuals, variations in the distribution of species and tem-


poral shifts in species proportions appear to be controlled by differences in physical conditions, such as flow rate and chemistry, but this control seems to be biologically mediated. While there is likely to be significant spatial and temporal variation in the development of physical conditions at specific vents, community changes should ultimately be interpretable within an orderly successional framework.

Conclusions Soft-bottom benthos occupy a

vast, continuous habitat character- ized by relatively low productivity and small-scale patchiness; low rates of fecundity, dispersal and successional change seem logical consequences. The contrasting rapid shifts in biomass and species structure at vents are made possible by the most unusual feature of these sites: high in situ productivity. The fast growth rates and high fecundities of vent megafauna (enabling long-range dispersal be- tween habitat islands) are sustain- able only through the remarkable levels of microbial chemosynthesis.

While some conclusions concerning colonization processes in the deep sea are possible, much re- mains to be learned about successional rates and mechanisms; study of natural disturbance regimes, colonization modes, and interspecific and organism-resource interactions are particularly necessary. In soft sediments, the frequency, scale and intensity of natural disturbance events remain poorly quantified, as do the rates of population increase resulting from alternative colonization modes (e.g. burrowing or crawl- ing of post-larval organisms versus larval recruitment). As in shallow water, the life stages of colonists may dictate the nature and out- come of interspecific interactions, and thus the mechanisms of succession33.

In order to address successional mechanisms at vents, disturbance regimes also require better documentation, especially with regard to physical changes precipitating fauna1 turnover. Finally, basic knowledge of the rates of fauna1 recruitment and utilization of resources (e.g. space, sulfides) at both new and old vents is sorely lacking. These gaps will best be filled by

time-series studies in specific soft- bottom and hydrothermal habitats. References I lumars, P.A. and Gallagher, E.D. ( 1982) in The Environment of the Deep Sea (Ernst, W. and Morin, I., eds), pp. 217-255, Prentice Hall 2 Grassle, J.F. and Sanders, H.L. (19731 Deep- Sea Res. 20,643-655 3 Grassle. I.F. 119861 Adv. Mar. Biol. 23, 301-361 4 jumars, P.A. ( 1981 I Mar. Mining 3,213-229 5 Grassle, I.F. (1977) Nature 265,618-619 6 Desbruyeres, D., Bervas, I.Y. and Khripounoff, A. (19801 Oteanol. A& 3,285-291 7 Desbruyeres, D., Deming, J.W., Dinet. A. and Khripounoff, A. (1985) in Peuplements Profonds du Golfe de Gascogne (Laubier. L. and Monniot, C., edsl, pp. 193-208, IFREMER (France) 8 Levin, L.A. and Smith, CR. II9841 Deep-Sea Res. 31, 1277-1285 9 Grassle, J.F. and Morse-Porteous, L.S. Deep- Sea Res. (in press) 10 McCall, P.L. 11977) J. Mar. Res. 35,221-226 II Zajac, R.N. and Whitlatch, R.B. (1982) Mar. Ecol. Progr. Ser. IO, 12-27 12 Pearson, T.H. and Rosenberg, R. ( 1978) Oceanogr. Mar. Biof. Annu. Rev. 16, 229-3 1 I 13 West, D.C. and Shugart, H.H. II981 1 Forest Succession: Concepts and Applications, Springer- Verlag I4 Smith, C.R. (1985) in Proc. 19th Eur. Mar. Biof. Symp. (Gibbs, P., ed.), pp. 183-189, Cambridge University Press 15 Turner, R.D. (1973) Science 180, 1377-1379 I6 Turner, R.D. ( I9771 Bull. Am. Malacol. Union 1976, 13-19

I7 Smith, CR. 11985) Deep-Sea Res. 32, 4 17-442 I8 Smith, C.R. (1986) 1. Mar. Res. 44, 567-600 I9 Mauviel, A. and Sibuet. M. II9851 in Peuplements Profonds du GolIe de Gastogne (Laubier, L. and Monniot, C.. edsl, pp. 157-173, IFREMER (France) 20 Young, D.K., lahn, W.H., Richardson, M.D. and Lohanick, A.W. ( I9851 Mar. Geol. 68, 269-30 I 21 Smith, CR.. jumars, P.A. and DeMaster, D.I. II9861 Nature 323,25 l-253 22 Brenchley, GA. ( 1981 I j. Mar. Res. 39, 767-790 23 Turk, T.R. and Risk, M.J. t 1981) Can. I. Fish. Aquat. Sci. 38,642-648 24 Sanders, H.L. ( 1979) Sarsia 64, l-7 25 Thistle, D., Yingst, 1.Y. and Fauchald, K. (1985)Mar.Geof.66,91-II2 26 Haymon. R.H. and Macdonald, K.C. I I9851 Am. Sci. 73,441-449 27 Hessler, R.R. and Smithey, W.M. II9831 in Hydrolhermal Processes at Seafloor Spreading Centers (Rona, P., Bostrom, K., Laubier, L. and Smith, K.L.. edsl, pp. 735-770. Plenum 28 Turner, R.D., Lutz, R.A. and Jablonski, D (1985) Bull. Biol. Sot. Wash. 6, 167-184 29 Berg, Cd. I I9851 Bull. Biol. SOL. Wash. 6. 185-197 30 Van Dover, C.L., Factor, J.R., Williams, A.B. and Berg, C.I. 119851 Bull. Biol. Sot. Wash. 6, 223-227 31 Hessler, R.R., Smithey, W.M. and Keller. C.H. f I9851 Bull. Biol. Sot. Wash. 6, 4 I l-428 32 lohnson. KS., Beehler, C.L.. Sakamoto- Arnold, C.M. and Childress, 1.1. II9861 Science 231,1139-l I41 33 Woodin, S.A. I I9761 1. Mar Res. 34, 25-4 I

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colonization and succession in deep-sea ecosystems

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